Top-down and bottom-up regulation in a high nutrient-high herbivory coastal ecosystem

Marine Ecology Progress Series

Volumn 432, Issue , 2011, Pages 69-82

  Martinetto, Paulina ^a,b   Teichberg, Mirta ^c   Valiela, Ivan ^d   Montemayor, Diana ^a,b   Iribarne, Oscar ^a,b  

^a UNIVERSIDAD NACIONAL DE MAR DEL PLATA   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c LEIBNIZ CENTRE FOR TROPICAL MARINE RESEARCH ZMT   (Germany)

^d ECOSYSTEMS CENTER   (United States)

Author keywords

Coastal eutrophication; Herbivory; Nutrients; Tidal influence; Top down vs. bottom up controls; Ulva lactuca

Indexed keywords

ABUNDANCE; ACCUMULATION RATE; ALGAL BLOOM; BIOACCUMULATION; BIOMASS; ENVIRONMENTAL DISTURBANCE; EUTROPHICATION; GREEN ALGA; HERBIVORY; MACROALGA; MARINE ECOSYSTEM; OXYGEN; PH; TROPHIC CONTROL; WATER EXCHANGE;

ARGENTINA; RIO NEGRO [ARGENTINA]; SAN ANTONIO BAY;

ALGAE; ULVA; ULVA LACTUCA;

EID: 79959729905     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps09173     Document Type: Article

References (80)

1. Aguiar AB, Morgan JA, Teichberg M, Fox S, Valiela I (2003) Transplantation and isotopic evidence of the relative effects of ambient and internal nutrient supply on the growth of Ulva lactuca. Biol Bull 205:250-251
2. Anderson TM, Dong Y, McNaughton SJ (2006) Nutrient acquisition and physiological responses of dominant Serengeti grasses to variation in soil texture and grazing. J Ecol 94:1164-1175 (Pubitemid 44511005)
3. Beer S, Israel A (1990) Photosynthesis of Ulva fasciata. IV. pH, carbonic anhydrase and inorganic carbon conversions in the unstirred layer. Plant Cell Environ 13:555-560
4. Borum J, Sand-Jensen K (1996) Is total primary production in shallow coastal marine waters stimulated by nitrogen loading? Oikos 76:406-410
5. Boyer EW, Goodale CL, Jaworski NA, Howarth RW (2002) Anthropogenic nitrogen sources and relationships to riverine nitrogen export in the northeastern USA. Biogeochemistry 57-58:137-169 (Pubitemid 34775870)
6. Bracken MES, Nielsen KJ (2004) Diversity of intertidal macro-algae increases with nutrient loading by invertebrates. Ecology 85:2828-2836 (Pubitemid 39448257)
7. Bracken MES, Stachowicz JJ (2007) Top-down modification of bottom-up processes: selective grazing reduces macro-algal nitrogen uptake. Mar Ecol Prog Ser 330:75-82
8. Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128-3139 (Pubitemid 44969263)
9. Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. BioScience 35: 634-639
10. Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210: 223-253 (Pubitemid 32164184)
11. 15N content of the opportunistic green macroalgae Enteromorpha intestinalis (Chlorophyta) to determine N sources to estuaries. J Phycol 41:287-293 (Pubitemid 40554889)
12. 15nitrogen in groundwater. Biogeochemistry 77:199-215 (Pubitemid 43248746)
13. Cruz-Rivera E, Hay M (2000) Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81:201-219 (Pubitemid 30086583)
14. D'Avanzo C, Kremer JN (1994) Diel oxygen dynamics and anoxic events in a eutrophic estuary of Waquoit Bay, Massachusetts. Estuaries 17:131-139 (Pubitemid 2098245)
15. Duarte CM (1995) Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 45:87-112
16. Flindt MR, Neto J, Amos CL, Pardal MA, Bergamasco A, Pedersen CB, Andersen FØ (2004) Plant bound nutrient transport. Mass transport in estuaries and lagoons. In: Nielsen SL, Banta GT, Pedersen MF (eds.) Estuarine nutrient cycling: the influence of primary producers. Kluwer Academic Publishers, Dordrecht, p 93-128
17. Fox SE, Teichberg M, Olsen YS, Heffner LE, Valiela I (2009) Restructuring of benthic communities in eutrophic estuaries: Lower abundance of prey leads to trophic shifts from omnivory to grazing. Mar Ecol Prog Ser 380:43-57
18. Fry B (2006) Stable isotope ecology. Springer-Verlag, New York, NY
19. Gearing PJ, Gearing JN, Maughan JT, Ovlatt CA (1991) Isotopic distribution of carbon sewage sludge and eutrophication in the sediments and food web of estuarine ecosystems. Environ Sci Technol 25:295-301
20. Geertz-Hansen O, Sand-Jensen K, Hansen DF, Christiansen A (1993) Growth and grazing control of abundance of the marine macroalga, Ulva lactuca L. in a eutrophic Danish estuary. Aquat Bot 46:101-109 (Pubitemid 24409406)
21. Giannotti AL, McGlathery KJ (2001) Consumption of Ulva lactuca (Chlorophyta) by the omnivorous mud snail Illyanassa obsoleta (Say). J Phycol 37:209-215 (Pubitemid 32391869)
22. Hemmi A, Jormalainen J (2004) Genetic and environmental variation in performance of a marine isopod: effects of eutrophication. Oecologia 140:302-311 (Pubitemid 39040087)
23. Holmes GT (2008) Nutrient supply, water residence time, temperature, and grazing as controls of size-fractionated phytoplankton biomass in shallow temperate estuarine ecosystems. PhD dissertation, Boston University, MA
24. Howarth RW (1988) Nutrient limitation of net primary production in marine ecosystems. Annu Rev Ecol Syst 19:89-110
25. Howarth RW, Billen G, Swaney D, Townsend A and others (1996) Regional nitrogen budget and riverine N and P fluxes for the drainages to the Atlantic Ocean: natural and human influences. Biogeochemistry 35: 75-139
26. Iribarne O, Martinetto P, Schwindt E, Botto F, Bortolus A, Garcia Borboroglu P (2003) Evidence of habitat displacement between two common soft-bottom SW Atlantic intertidal crabs. J Exp Mar Biol Ecol 296:167-182 (Pubitemid 37274198)
27. Isacch JP, Costa CS, Rodríguez-Gallego L, Conde D, Escapa M, Gagliardini DA, Iribarne O (2006) Distribution of salt-marsh plant communities associated with environmental factors along a latitudinal gradient on the SW Atlantic coast. J Biogeogr 33:888-900
28. Korpinen S, Honkanen T, Vesakoski O, Hemmi A, Koivikko R, Loponen J, Jormalainen V (2007) Macroalgal communities face the challenge of changing biotic interactions: review with focus on the Baltic Sea. Ambio 36:203-211 (Pubitemid 46942192)
29. Lapointe BE, Tenore KR (1981) Experimental outdoor studies with Ulva fasciata Delile. I. Interaction of light and nitrogen on nutrient uptake, growth, and biochemical composition. J Exp Mar Biol Ecol 53:135-152
30. Lapointe BE, Littler MM, Littler DS (1992) Nutrient availability to marine macroalgae in siliciclastics versus carbonaterich coastal waters. Estuaries 15:75-82
31. Larsson C, Axelsson L (1999) Bicarbonate uptake and utilization in marine macroalgae. Eur J Phycol 34:79-86 (Pubitemid 29178010)
32. Larsson C, Axelsson L, Ryberg H, Beer S (1997) Photosynthetic carbon utilization by Enteromorpha intestinalis (Chlorophyta) from a Swedish rockpool. Eur J Phycol 32: 49-54
33. Lotze HK, Worm B (2000) Variable and complementary effects of herbivores on different life stages of bloomforming macroalgae. Mar Ecol Prog Ser 200:167-175
34. Lubchenco J (1978) Plant species diversity in a marine intertidal community: importance of herbivore food preference and algal competitive abilities. Am Nat 112:23-39
35. Martinetto P, Teichberg M, Valiela I (2006) Coupling of estuarine benthic and pelagic food webs to land-derived nitrogen sources in Waquoit Bay, Massachusetts, USA. Mar Ecol Prog Ser 307:37-48 (Pubitemid 43293997)
36. Martinetto P, Daleo P, Escapa M, Alberti J and others (2010) High abundance and diversity of consumers associated with eutrophic areas in a semi-desert macrotidal coastal ecosystem in Patagonia, Argentina. Estuar Coast Shelf Sci 88: 357-364
37. McClelland JM, Valiela I (1998) Linking nitrogen in estuarine producers to land-derived sources. Limnol Oceanogr 43: 577-585 (Pubitemid 28382167)
38. McGlathery KJ (1995) Nutrient and grazing influences on a subtropical seagrass community. Mar Ecol Prog Ser 122: 239-252 (Pubitemid 26449944)
39. McGlathery KJ, Marino R, Howarth RW (1994) Variable rates of phosphate uptake by shallow marine carbonate sediments: mechanisms and ecological significance. Biogeochemistry 25:127-146 (Pubitemid 2114026)
40. McGlathery KJ, Krause-Jensen D, Rysgaard S, Christensen PB (1997) Patterns of ammonium uptake within dense mats of the filamentous algae Chaetomorpha linum. Aquat Bot 59:99-115 (Pubitemid 28114344)
41. McGlathery KJ, Sundbäck K, Anderson IC (2007) Eutrophication in shallow coastal bays and lagoons: the role of plants in the coastal filter. Mar Ecol Prog Ser 348:1-18 (Pubitemid 350189904)
42. Menge BA (1992) Community regulation: Under what conditions are bottom-up factors important on rocky shores? Ecology 73:755-765
43. Monbet Y (1992) Control of phytoplankton biomass in estuaries: a comparative analysis of macrotidal and microtidal estuaries. Estuaries 15:563-571 (Pubitemid 23402963)
44. Morgan JA, Aguiar AB, Fox S, Teichberg M, Valiela I (2003) Relative influence of grazing and nutrient supply on growth of the green macroalga Ulva lactuca in estuaries of Waquoit Bay, Massachussetts. Biol Bull 205:252-253
45. 15N accumulation in algal tissue. J Phycol 38:135-144 (Pubitemid 34196837)
46. Nixon SW (1995) Coastal marine eutrophication: a definition, social causes and future concerns. Ophelia 41:199-219
47. Oczkowski O, Nixon S, Henry K, DiMilla P and others (2008) Distribution and trophic importance of anthropogenic nitrogen in Narragansett Bay: an assessment using stable isotopes. Estuar Coasts 31:53-69 (Pubitemid 351912675)
48. Pace ML, Findlay SEG, Lints D (1992) Zooplankton in advective environments: the Hudson River community and a comparative analysis. Can J Fish Aquat Sci 49:1060-1069
49. Pascual MS, Zampatti EA, Iribarne O (2001) Population structure and demography of the Puelche oyster (Ostrea puelchana, D'Orbigny) grounds in northern Patagonia, Argentina. J Shellfish Res 20:1003-1010 (Pubitemid 34209473)
50. Peckol P, Demeoanderson B, Rivers J, Valiela I, Maldonado M, Yates J (1994) Growth, nutrient uptake capacities and tissue constituents of the macroalgae Cladophora vagabunda and Gracilaria tikvahiae related to site-specific nitrogen loading rates. Mar Biol 121:175-185
51. Pedersen MF, Borum J (1996) Nutrient control of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Mar Ecol Prog Ser 142:261-272
52. Pedersen MF, Borum J (1997) Nutrient control of estuarine macroalgae: growth strategy and the balance between nitrogen requirements and uptake. Mar Ecol Prog Ser 161: 155-163 (Pubitemid 28094350)
53. Porter KG (1976) Enhancement of algal growth and productivity by grazing zooplankton. Science 192:1332-1334
54. Raffaelli DG, Raven JA, Poole LJ (1998) Ecological impact of green macroalgal blooms. Oceanogr Mar Biol Annu Rev 36: 97-125
55. Runcie JW, Ritchie RJ, Larkum AW (2003) Uptake kinetics and assimilation of inorganic nitrogen by Catenella nipae and Ulva lactuca. Aquat Bot 76:155-174 (Pubitemid 36632004)
56. Ryther JH, Dunstan WM (1971) Nitrogen, phosphorus and eutrophication in the coastal marine environment. Science 171: 1008-1013
57. Sfriso A, Pavoni B, Marcomini A, Orio AA (1992) Macroalgae, nutrient cycles, and pollutants in the Lagoon of Venice. Estuaries 15:517-528 (Pubitemid 23402945)
58. Shaw RG, Mitchell-Olds T (1993) ANOVA for unbalanced data: an overview. Ecology 74:1638-1645 (Pubitemid 24408335)
59. Smith VH, Schindler DW (2009) Eutrophication science: where do we go from here? Trends Ecol Evol 24:201-207
60. Solidoro C, Bandelj V, Bernardi FA, Camatti E and others (2010) Response of the Venice lagoon ecosystem to natural and anthropogenic pressures over the last 50 years. In: Kennish MJ, Pearl HW (eds.) Coastal lagoons: critical habitats of environmental change. CRC Press, Boca Raton, FL, p 483-511
61. Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799-801
62. Sterner RW (1986) Herbivores' direct and indirect effects on algal populations. Science 231:605-607
63. Strickland JDH, Parsons TR (1968) A manual for sea water analysis. Bull Fish Res Board Can 167
64. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis, 2nd edn. J Fish Res Board Canada 167
65. Teichberg M (2007) Macroalgal growth: local and global comparisons of nutrient limitation and assimilation. PhD dissertation, Boston University, MA
66. Teichberg M, Heffner LR, Fox S, Valiela I (2007) Nitrate reductase and glutamine synthetase activity, internal N pools, and growth of Ulva lactuca: responses to long and short-term N supply. Mar Biol 151:1249-1259 (Pubitemid 46682903)
67. Teichberg M, Fox S, Aguila C, Osen Y, Valiela I (2008) Macroalgal response to experimental nutrient enrichment in shallow coastal waters: growth, internal nutrient pools, and isotopic signature. Mar Ecol Prog Ser 368:117-126
68. Teichberg M, Fox SE, Olsen YS, Valiela I and others (2010) Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp. Glob Change Biol 16:2624-2637
69. Thomas TE, Harrison PJ (1987) Rapid ammonium uptake and nitrogen interactions in five intertidal seaweeds grown under field conditions. J Exp Mar Biol Ecol 107:1-8
70. Thomsen MS, McGlathery KJ (2007) Stress tolerance of the invasive macroalgae Codium fragile and Gracilaria vermiculophylla in a soft-bottom turbid lagoon. Biol Invasions 9:499-513 (Pubitemid 46944646)
71. Valentine JF, Heck KL Jr (2001) The role of leaf nitrogen content in determining turtlegrass (Thalassia testudinum) grazing by a generalized herbivore in the northeastern Gulf of Mexico. J Exp Mar Biol Ecol 258:65-86 (Pubitemid 32220677)
72. Valiela I (1995) Marine ecological processes. Springer-Verlag, New York, NY
73. Valiela I (2006) Global coastal change. Blackwell Publishing, Malden, MA
74. Valiela I, Foreman K, LaMontagne M, Hersh D and others (1992) Couplings of watersheds and coastal waters: sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts. Estuaries 15:443-457 (Pubitemid 23402964)
75. Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci USA 105: 15452-15457
76. Viaroli P, Bartoli M, Bondavalli C, Christian RR, Giordani G, Naldi M (1996) Macrophyte communities and their impact on benthic fluxes of oxygen, sulphide and nutrients in shallow eutrophic environments. Hydrobiologia 329: 105-119 (Pubitemid 26399551)
77. Vymazal J (1995) Algae and elemental cycling in wetlands. Lewis Publishers, Boca Raton, FL
78. Williamson JE, Rees TAV (1994) Nutritional interaction in an algae-barnacle association. Oecologia 99:16-20
79. 2.Geochim Cosmochim Acta 59:107-114
80. Zieman JC, Iverson RL, Ogden JC (1984) Herbivory effects on Thalassia testudinum leaf growth and nitrogen content. Mar Ecol Prog Ser 15:151-158